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How Does Mytilus Galloprovincialis Respond When Exposed to the Gametophyte Phase of the Invasive Red Macroalga Asparagopsis Armata Exudate?

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How Does Mytilus Galloprovincialis Respond When Exposed to the Gametophyte Phase of the Invasive Red Macroalga Asparagopsis Armata Exudate? water Article How Does Mytilus galloprovincialis Respond When Exposed to the Gametophyte Phase of the Invasive Red Macroalga Asparagopsis armata Exudate? Sónia D. Coelho * , Hugo C. Vieira, Jacinta M. M. Oliveira ,Sílvia F. S. Pires , Rui J. M. Rocha , Andreia C. M. Rodrigues , Amadeu M. V. M. Soares and Maria D. Bordalo CESAM (Centre for Marine and Environmental Studies), Department of Biology, University of Aveiro, 3810-193 Aveiro, Portugal; [email protected] (H.C.V.); [email protected] (J.M.M.O.); [email protected] (S.F.S.P.); [email protected] (R.J.M.R.); [email protected] (A.C.M.R.); [email protected] (A.M.V.M.S.); [email protected] (M.D.B.) * Correspondence: [email protected] Abstract: Asparagopsis armata is classified as an invasive species in Europe. Through the exudation of secondary metabolites, this macroalga holds a chemical defence against consumers, with potential toxic effects to native rocky shore communities. This study aims to evaluate the potential impact of A. armata (gametophyte) exudate in a native species, the mussel Mytilus galloprovincialis, in terms of biochemical and organismal effects. The 96 h-LC50 was 3.667% and based on it, exudate concentrations (0.25; 0.5; 1; 2%) were determined to further sublethal experiments. These sublethal concentrations caused no oxidative damage in the digestive gland since lipid peroxidation and Citation: Coelho, S.D.; Vieira, H.C.; protein carbonylation were not affected. Nevertheless, there was a significant rise in the electron Oliveira, J.M.M.; Pires, S.F.S.; Rocha, transport system activity and total glutathione content in muscle, suggesting an increased non- R.J.M.; Rodrigues, A.C.M.; Soares, enzymatic antioxidant capacity and consequent energy consumption to cope with potential pro- A.M.V.M.; Bordalo, M.D. How Does oxidant compounds. This might have contributed to the observed decline in cellular energy allocation Mytilus galloprovincialis Respond of the exposed mussels. At the organismal level, clearance capacity declined along the concentration When Exposed to the Gametophyte gradient. Moreover, the number of functional byssuses decreased with increasing concentrations and Phase of the Invasive Red Macroalga Asparagopsis armata Exudate? Water a significant reduction in their attachment strength was observed. These findings suggest that the 2021, 13, 460. https://doi.org/ presence of A. armata may compromise M. galloprovincialis integrity in the invaded coastal areas. 10.3390/w13040460 Keywords: invasive macroalgae; marine; biochemical markers; clearance rate; byssus production Academic Editor: María Pilar Cabezas Rodríguez Received: 21 January 2021 Accepted: 6 February 2021 1. Introduction Published: 10 February 2021 The continuous proliferation of invasive seaweeds has grown a great concern consider- ing their impacts on native marine communities, mainly because they naturally threaten the Publisher’s Note: MDPI stays neutral availability of resources compromising the natural ecosystem functioning [1]. The red ma- with regard to jurisdictional claims in rine macroalgae Asparagopsis armata Harvey, 1855 (Bonnemaisoniales, Rhodophyta), native published maps and institutional affil- from southern Australia and New Zealand, is identified as an invasive species and widely iations. distributed in the Mediterranean and Atlantic coasts of Europe including Portugal [2,3]. This temperate alga can overcome the ecological barriers and colonise diverse environmen- tal conditions, mainly due to its fast growth rate, lack of predators and its effective spread, both through the tetrasporophyte floating balls and the gametophyte phase that hooks onto Copyright: © 2021 by the authors. floating material [4,5]. A. armata sets mainly in the coastal low intertidal zone extending to Licensee MDPI, Basel, Switzerland. the upper meters of the subtidal zone [3,6]. Therefore, it competes for resources (mainly This article is an open access article space and nutrients) with specific native species, such as epifaunal assemblages. Further- distributed under the terms and more, this macroalga is adapted to strong physicochemical changes [7,8], characteristic conditions of the Creative Commons from this zone, imposed by wave action and the ebb and flow of the tide. These tidal Attribution (CC BY) license (https:// cycles lead to the formation of microenvironments within intertidal tide pools, wherein the creativecommons.org/licenses/by/ organisms face adverse conditions [9]. Like other seaweeds (particularly concerning in case 4.0/). Water 2021, 13, 460. https://doi.org/10.3390/w13040460 https://www.mdpi.com/journal/water Water 2021, 13, 460 2 of 16 of invasive macroalgae [10,11]), A. armata is known to exude a wide array of secondary metabolites with potentially deleterious effects, including a large number of halogenated compounds (e.g., haloketones, haloacids and haloforms) [12,13]. This mixture is usually produced as a chemical defence against consumers, epiphytes such as bacteria and may act in space competition (allelopathy) [4,14]. Exudation of such compounds may therefore cause toxic effects to surrounding species which together with the competition for natural resources, especially in the intertidal tide pools, can enhance the impacts of A. armata on ecosystem integrity and functioning. Given this potential as an ecosystem engineer, very common to marine macroalgae [15], it is crucial to evaluate this non-indigenous alga’ ef- fects. Although few studies addressed this problem, little is known about it. For example, it was demonstrated that A. armata halogenated metabolites deterred feeding by two marine mesograzers (Hyale nigra and juvenile abalone Haliotis rubra)[16]. Exposure to its exudate caused physiological status impairment in exposed Palaemon elegans and Gibbula umbilicalis, as well as feeding inhibition in this gastropod [17]. There is limited knowledge on the impact of toxic secondary metabolites derived from macroalgae on bivalve species, contrary to the deleterious effects of bioactive compounds and toxins produced by cyanobacteria and dinoflagelates, e.g., [18–20]. Nonetheless, the physiological status of the mussel Pinna nobilis was found to be negatively affected when colonized by the invasive red macroalga Lophlocladia lallemandi, which is known to produce lophocladines with potential cytotoxic effects [21]. Thereby, the present study arises at as- sessing possible effects of A. armata exudates on the native mussel Mytilus galloproviancialis Lamarck, 1819. This species forms large and dense mono-and multi-layered beds in the low to mid intertidal rocky shores [22,23]. M. galloprovincialis has been employed as a sentinel species for monitoring coastal environments due to its widespread distribution, abundance and sedentary lifestyle [24–27]. They have an impressive filter-feeding behaviour, being capable to uptake several waterborne contaminants, thus reflecting the impacts of different environmental disturbances, e.g., [28–31]. Furthermore, M. galloprovincialis has great eco- logical relevance in coastal ecosystems by playing a critical role in the water quality through the filtration of particles and excess nitrogen from the aquatic environment [32,33]. They are also considered important links in coastal trophic chains between bottom-dwelling organisms and phytoplankton [32]. In addition, mussel beds contribute to increasing habitat complexity and therefore biodiversity [34,35], by providing shelter to a variety of organisms and nurseries of juvenile fish and crustaceans. Therefore, eventual ecologi- cal consequences may derive from M. galloprovincialis decline. Aside from its ecological importance, M. galloprovincialis has a high economic value, both in Portugal and world- wide. It is considered an important food resource for human consumption, thus being among the most harvested species and representing a significant part in the overall marine aquaculture [32,36–38]. In this sense, this work intends to understand how this mussel species respond in the presence of A. armata exudate, by evaluating its toxicity in terms of biochemical and organismal responses. 2. Materials and Methods 2.1. Asparagopsis armata Sampling and Exudate Production A. armata (gametophyte phase) was collected by hand through free diving in the subtidal zone at the Terceira island Azores (Portugal) (38◦38059.200 N, 27◦13016.400 W) in January 2019. The macroalgae were kept in aerated seawater tanks until next day and packed in sealed containers to be transported to the laboratory in Aveiro (Portugal). Immediately upon arrival, A. armata was cleared from visibly associated fauna and allocated to a tank with artificial seawater (marine RedSea® Salt premium grade) in a 1:10 proportion (salinity 35 ± 1, pH 8.0 ± 0.1, temperature 20.0 ± 0.5 ◦C) in the dark and no aeration for 24 h to produce the exudate, adapted from [39–41]. These conditions were previously optimized to obtain exudate from the stressed alga without causing its death during the process. Afterwards, the Water 2021, 13, 460 3 of 16 alga was removed from the tank and the resulting media (considered as the stock solution and representing 100% of exudate) was preserved at −20 ◦C, until further use. 2.2. Mytilus galloprovincialis Sampling and Acclimatization M. galloprovincialis specimens (4 ± 0.5 mm length), were collected by hand, during low tide, from the intertidal rocky shores of the Barra de Aveiro (Portugal) (40◦38038.800 N, 8◦44044.600 W). Organisms were transported from the field to the laboratory and were immediately cleaned of superficial
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